ARTICLE IN PRESS

Journal of Biomechanics 38 (2005) 1932–1937

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Technical note

Is the force-length relationship a useful indicator of contractile

element damage following eccentric exercise?
Timothy A. Butterfield, Walter Herzog
Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, 2500 University Drive NW, Calgary, Alta. Canada T2N 1N4
Accepted 11 August 2004

Abstract

Eccentric exercise has been shown to have a measurable effect on the force–length relationship (FLR), as peak force is shifted to
longer muscle lengths following exercise. Recently, this shift in the FLR has been proposed as a ‘‘simple, reliable indicator’’ for
assessing contractile element damage following eccentric exercise. However, eccentric exercise causes fatigue and damage, and there
is evidence that fatigue alone may also cause a shift in the FLR. The purpose of this paper was to assess the role of fatigue on the
FLR (as measured by a torque–joint angle relationship) following isometric and eccentric exercise in the New Zealand white (NZW)
rabbit. Six NZW rabbits were divided into two groups for eccentric or isometric contractions of the hindlimb dorsiflexor muscles.
Pre- and post-exercise torque–joint angle relationships were measured, and the shift from the pre- to the post-exercise relationship
was measured as the change in joint angle at which peak torque was produced. Eccentric exercise resulted in a rightward shift of
seven degrees; isometric exercise, which is thought to not cause damage, resulted in a shift of four degrees. Furthermore, torque
production was reduced to a greater extent at short compared to long muscle lengths for the eccentric and isometric exercise,
resulting in a post-exercise torque–joint angle relationship that was altered in shape. We conclude from these results, that the shift in
peak torque may not be a simple and reliable indicator of muscle damage, but is caused by a combination of damage and post-
exercise fatigue.
r 2004 Elsevier Ltd. All rights reserved.

Keywords: Muscle; Force–length relationship; Eccentric; Isometric; Fatique

1. Introduction (Brockett et al., 2001; Morgan and Allen, 1999; Morgan

Eccentric exercise has been shown to have a measurable
effect on the force–length relationship (FLR), as peak
force is produced at a longer muscle length following
exercise (Talbot and Morgan, 1996; Jones et al., 1997;
Wood et al., 1993). Several mechanisms producing this
rightward shift in the FLR following exercise have been
proposed. These include stretch-induced damage to
calcium handling structures, (Balnave and Allen, 1995;
Warren et al., 1993; Endo, 1972), visco-elastic creep
(Fowles et al., 2000) , and contractile element damage
Corresponding author. Tel: +1-403-220-8525; fax: +1-403-284-
3553.
E-mail address: walter@kin.ucalgary.ca (W. Herzog).
et al., 1996; Brockett et al., 2002). Recently, the rightward
shift in the FLR has been proposed as a ‘‘simple, reliable
indicator’’ for assessing contractile element damage
following eccentric exercise (Whitehead et al., 2003).
The rightward shift in the FLR was first identified
with contractile element injury by Katz (1939), who
proposed that contractile elements were transformed
into passive elastic elements by muscle stretch. Morgan
(1990) proposed that this transformation of contractile
elements during eccentric contractions occurs through a
‘popping’ of a small number of sarcomeres as they are
stretched beyond myofilament overlap, resulting in an
increase in muscle compliance. As a consequence, the
muscle would produce peak force at a longer length,
thereby exhibiting a rightward shift of the FLR.

0021-9290/$ - see front matter r 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jbiomech.2004.08.013
 ARTICLE IN PRESS
T.A. Butterfield, W. Herzog / Journal of Biomechanics 38 (2005) 1932–1937
This rightward shift of the FLR following eccentric
contractions has been observed in a variety of studies
and muscle preparations, including human plantarflex-
ors (Whitehead et al., 1998; Jones et al., 1997), and
hamstrings (Brockett et al., 2001), single toad fibers
(Jones et al., 1997), single frog fibers (Morgan et al.,
1996), and individual motor units from the cat medial
gastrocnemius (Brockett et al., 2002). In each of these
studies, the shift was associated with contractile element
damage. In addition, histological findings post-exercise
supported the concept of contractile element injury
within the muscle following eccentric exercise (Jones et
al., 1997), although the possible contribution of fatigue
on the FLR was not considered.
Unlike eccentric contractions, isometric exercise does
not produce extensive contractile element damage (Koh
and Brooks, 2001), and presents a unique model to
study the effects of fatigue on the FLR in the absence of
muscle injury. Although previous studies have assessed
the effects of fatigue on the force–length relationship,
the use of single fibers (Yeung et al., 2002a, b) or lack of
direct comparison to the post eccentric exercise FLR
(Cutlip et al., 2004) leaves the contribution of fatigue to
the rightward shift of the FLR following eccentric
exercise unclear. Therefore, the purpose of this study
was to directly test the hypothesis that fatigue con-
tributes to the rightward shift in the FLR of the ankle
dorsiflexors in New Zealand white rabbits following
eccentric exercise.
2. Materials and methods
2.1. Experimental design
Eight skeletally mature NZW rabbits (5.670.2 kg,
Riemens, St. Agatha, Ontario, Canada) were divided
into two study groups for measurement of a pre-exercise
and post-exercise torque–joint angle relationship.
Group one consisted of five rabbits (nine hindlimbs)
subjected to eccentric exercise. Group two consisted of
three rabbits (six hindlimbs) subjected to an equivalent
isometric exercise. All procedures were approved by the
Animal Care Committee of the University of Calgary.
2.2. Surgical procedure
Rabbits were tranquilized with 0.18 ml (10 mg/ml)
acepro-25 (MTC Pharmaceuticals, Cambridge, ON,
Canada) and held under anesthesia with 1.5% isoflur-
ane, 0.6 L/min N2O and 0.8 L/min O2. An incision was
made on the posterior aspect of the right and left
hindlimbs, anterior to the sciatic vein, and the biceps
femoris and semimembranosis were separated exposing
the peroneal nerve. Nerve cuff stimulating electrodes
were secured over the right and left common peroneal
1933
nerves, superior to the gastrocnemius and distal to the
branching of the sciatic nerve. In this manner, all
dorsiflexors of the tibiotarsal joints were stimulated
effectively. Following implantation, the skin was stapled
closed.
2.3. Exercise and measurement protocol
2.3.1. Eccentric exercise, group 1
Rabbits were placed supine in a stereotaxic frame
with the knee at 901 flexion (full extension=01). The
foot was strapped to a servo-motor footplate (Parker
Hannifin Corporation, Irwin, PA, USA) and ankle
movement was controlled via computer (Motion Plan-
ner, Rohnert Park, CA, USA). The tibiotarsal
joint angle was set at 901 (full extension=1801) which
served as the reference angle for the remainder of
the experiment. The peroneal nerve cuff leads were
attached to a stimulator (Grass S8800, Astro-Med
Inc., Longueil, QC, Canada), and the a-motoneuron
threshold was determined (pulse duration=0.1 ms,
frequency=150 Hz).
First, a pre-exercise, isometric torque–joint angle
relationship was determined by supramaximally stimu-
lating (3  a-motoneuron threshold voltage, pulse dur-
ation=0.1 ms, frequency=150 Hz, train duration=
2000 ms) the dorsiflexor muscles, beginning at a
tibiotarsal angle of 551 and progressing in 51 increments
to 1551. To limit the potential effects of creep of passive
elements at long muscle lengths, the foot was parked at a
551 joint angle (short muscle length) between isometric
contractions. Therefore, following each isometric con-
traction, the foot was returned passively to a dorsiflexed
position (551 tibiotarsal angle) for 2 min of rest between
contractions.
The exercise protocol consisted of eccentric contrac-
tions performed from a tibiotarsal angle of 70–1051 of
plantar flexion at 701 s 1(3  a-motoneuron threshold
voltage, pulse duration=0.1 ms, frequency=150 Hz,
train duration=500 ms). Each stretch-shortening cycle
lasted 1000 ms. Stimulation started at the onset of
plantar flexion and ceased at the end of the eccentric
exercise (1051), resulting in an eccentric exercise of
500 ms duration. Immediately following the eccentric
contraction, the foot was passively returned to the 701
starting position at 701 s 1(500 ms passive shortening).
To induce muscle injury associated with eccentric
contractions, it has been shown that greater than one
contraction is required when working within the
physiologic range of motion (Cutlip et al., 2004;
Gosselin and Burton, 2002). Therefore, the exercise
protocol consisted of five sets of ten eccentric contrac-
tions, with 2 min rest between sets. Immediately after the
eccentric protocol, a post-exercise torque-joint angle
relationship was measured in a manner identical to the
pre-exercise relationship. However, the rest between
 ARTICLE IN PRESS
1934 T.A. Butterfield, W. Herzog / Journal of Biomechanics 38 (2005) 1932–1937
isometric contractions was reduced to 30 s to limit the
recovery from fatigue during measurement of the FLR
post-exercise. Therefore, the foot was returned to a
dorsiflexed position (551 tibiotarsal joint angle) between
contractions, but for only 30 s of rest before moving to
the next joint angle.
2.3.2. Isometric exercise, group 2
Using identical stimulation parameters as described
above, the pre-exercise torque–joint angle relationship
was measured. Then, isometric contractions (3x a-
motoneuron threshold voltage, pulse duration=0.1 ms,
frequency=150 Hz, train duration=500 ms, 500 ms rest)
were performed at a tibiotarsal angle of 951. This joint
angle was chosen for the isometric contractions for
several reasons: Firstly, pilot data indicated that it was,
on average, the angle at which peak isometric torque
was produced by the dorsiflexors; secondly, it lies within
the range of motion for our eccentric protocol; and
lastly, we found that little or no passive tension was
associated with this muscle length, thus limiting the
effects of creep during testing. The 500 ms train
duration, and 500 ms rest between contractions in each
protocol, assured that stimulation duration and timing
were identical between the two exercise groups. The
protocol consisted of five sets of 10 isometric contrac-
tions with 2 min rest between sets. A post-exercise
torque–joint angle relationship was measured immedi-
ately following exercise as described above.
2.4. Torque-joint angle evaluation
Two precision strain gauges (Vishay Micro-Measure-
ments, Raleigh, NC, USA. Item No. CEA-06-125WT-
350) were arranged in a full bridge configuration,
creating an instrumented cam connecting the footplate
to the motor. Strain gauge calibration confirmed the
linearity of output voltage as a function of strain
(R240.99) through a range greater than required for
our protocol. The output signal was routed through
a strain gauge amplifier/conditioner (Vishay 2100,
Vishay Micro-Measurements, Raleigh, NC, USA. Gain
8.44  100; Excitation 10 Vdc; low pass filter 10 Hz) and
sampled at 250 Hz with WinDaq data acquisition
software (Dataq Instruments, Akron, Ohio, USA).
Peak torque values were plotted for all 21 tibiotarsal
joint angles. Mean torques across all joints were plotted
pre- and post-exercise. In order to calculate the angle of
peak torque occurrence, torque values475% of the
absolute peak torque were normalized, fit with a second-
order polynomial, and peak torque was calculated as the
peak value of the polynomial approximation. In
addition, the mean rightward shift, calculated as the
average of the shifts for each subject, was calculated for
comparison (Jones et al., 1997; Whitehead et al., 2001).
For force decrement data, post-exercise torques were
expressed as a percent decrease from the pre-exercise
values. All statistical analyses were performed using
SPSS version 11.5 (SPSS Incorporated, Chicago, IL,
USA). For all parameters measured, means7SE are
reported. Statistical significance was set at po0.05, and
analyzed using Student’s paired, or independent, t-tests.
3. Results
Following eccentric exercise, peak torque values at all
angles were significantly lower compared to those
obtained pre-exercise for all joint angles measured
(po0.001, Fig. 1). Analysis of the torque–angle relation-
ships revealed a rightward shift for all subjects in the
eccentric group, and all but one subject in the isometric
group (Table 1). Overall, mean peak torque production,
as calculated from the polynomial fitted to the mean
torque values following eccentric exercise, occurred at a
joint angle of 1041 compared to the pre-exercise peak of
981, resulting in a 61 rightward shift. The rightward shift
calculated as the average of individual fitted polyno-
mials was 71 (Table 1). In addition, the shape of the
torque-angle relationship was rotated in a counter-
clockwise manner following eccentric exercise (Fig. 1,
inset).
Following isometric exercise, peak torque values at all
angles were significantly lower compared to those
obtained pre-exercise for all joint angles measured
(po0.001, Fig. 2). Analysis of joint torque decrement
between protocols revealed the greatest decrement in
joint torque production following isometric exercise was
40.573.0% at a tibiotarsal joint angle of 601. The
greatest torque decrement following eccentric exercise
was 55.073.0%, and was measured at the smallest
tibiotarsal joint angle, 551 (Fig. 3). Torque decrement
following eccentric exercise was not significantly differ-
ent compared to the decrement following isometric
exercise, except at short muscle lengths (po0.002),
corresponding to the smallest joint angles (55–701,
Fig. 3). The mean peak torque value, calculated from
the polynomial fitted to the mean torque values
following isometric exercise, was shifted to the right
by four degrees, from 1011 to 1051, and the curve
was rotated in a counterclockwise direction (Fig. 2,
inset). Calculating the rightward shift as the average
of individual shifts resulted in a mean rightward shift of
31, (Table 1).
4. Discussion
Although a rightward shift in the FLR has been
associated with histological evidence of contractile
element damage following eccentric exercise, the results
of this study suggest that a portion of the rightward shift
 ARTICLE IN PRESS
T.A. Butterfield, W. Herzog / Journal of Biomechanics 38 (2005) 1932–1937 1935

1.1
1.0 R2 = 0.98
R2 = 0.99
0.9
1.2
0.8
0.7
1.0 0.6
0.5
Joint Torque [Nm]

60 70 80 90 100 110 120 130 140

0.8

0.6

0.4

0.2

0.0
50 60 70 80 90 100 110 120 130 140 150 160
Tibiotarsal Joint Angle [degrees]

Fig. 1. Torque–angle relationship for NZW dorsiflexors before (J) and after () a bout of eccentric exercise. Note the apparent shift to the right in
peak force production (from 100 to 1051) and the change in shape of the torque-joint angle relationship following exercise. Torque production
following eccentric exercise was significantly reduced compared to pre-exercise values at all joint angles tested (po0.001). Values are mean7SE
(n=9). Inset. Normalized torque–angle relationship. Here the rightward shift and counterclockwise rotation are evident. Data were fitted with a
second-order polynomial to calculate the angle of peak torque production pre-exercise (981) and post-exercise (1041).

Table 1 to 43% by calculating the shift as the mean shift

Shift in peak torques from pre- to the post-exercise torque–angle obtained from the individual subjects (Table 1).
relationship for individual subjects in the eccentric and isometric test
groups.
Jones et al. (1997) also observed a rightward shift in
the FLR using passive stretch combined with isometric
Eccentric Shift in Peak Isometric Shift in Peak exercise in human plantar flexor muscles that amounted
exercise Torque Exercise Torque to 50% of the shift following an eccentric exercise
ECC1L +71 ISO1L +31 protocol. However, the authors deemed the isometric
ECC2L +41 ISO1R +31 shift insignificant. In the same paper, a significant
ECC2R +71 ISO2L 01 rightward shift in optimum force production of 3.5%
ECC3L +121 ISO2R +51 muscle length was also reported for single toad fibers
ECC3R +41 ISO3L +31
following a protocol of passive stretch and isometric
ECC4L +91 ISO3R +31
ECC4R +121 contractions (Jones et al., 1997). Although these results
ECC5L +41 are similar to ours, a direct comparison is difficult as the
ECC5R +51 use of passive stretch may have produced damage (Koh
MEAN +71 MEAN +31 and Brooks, 2001), that could have contributed to the
A positive value indicates a rightward shift of the peak torque towards shift.
increased muscle lengths. The mean rightward shift was calculated as Other studies have reported conflicting results com-
the average of the individual shift values. ECC=eccentric, pared to those presented here. Whitehead et al. (2003)
1,2,3,4,5=subject number; L, R=left and right. ISO=isometric, showed a small shift in peak force production following
1,2,3=subject number; L,R,=left and right.
isometric exercise in the cat medial gastrocnemius,
which would only account for a small proportion of
the shift reported following eccentric exercise (o10%).
and change in shape of the torque–angle relationship However, their fatigue protocols resulted in much
after exercise is contributed by the effects of fatigue. In smaller force decrements at optimal length following
our study, the isometric exercise resulted in a rightward exercise (7% and 13%) compared to ours (29%).
shift of 41 fitting mean torque values with one Conversely, single fiber experiments have shown no
polynomial (Fig. 2). This amounts to 67% of the 61 shift in peak force production following isometric
rightward shift obtained following the eccentric exercise exercise (Yeung et al., 2002a). However, a direct
protocol using the same procedure (Fig. 1). The overall comparison between their in vitro protocol and our
contribution of fatigue to the rightward shift is reduced study is difficult.
 ARTICLE IN PRESS
1936 T.A. Butterfield, W. Herzog / Journal of Biomechanics 38 (2005) 1932–1937

1.1

1 2 2
R = 0.98 R = 0.99
0.9

0.8
1.6
0.7

1.4 0.6
0.5
1.2 60 70 80 90 100 110 120 130 140
Joint Torque [Nm]

0.8

0.6

0.4

0.2

0
50 60 70 80 90 100 110 120 130 140 150 160
Tibiotarsal Joint Angle [degrees]

Fig. 2. Torque–angle relationship for NZW dorsiflexors before (J) and after () a bout of isometric exercise. Note the apparent lack of rightward
shift in peak force production (1051). Torque production following isometric exercise was significantly reduced compared to pre-exercise values at all
joint angles tested (po0.001). Values shown are mean7SE (n=6). Inset. Normalized torque-angle relationship. Here the rightward shift and
counter-clockwise rotation are evident. Data were fitted with a second order polynomial to calculate the angle of peak torque production pre-exercise
(1011) and post-exercise (1051).

70 following both eccentric exercise (Fig. 1, inset) and

isometric exercise (Fig. 2, inset). Decreased isometric
Post Exercise Torque Decrement [%]

60 * force production has been shown to be greatest at short

*
*
* muscle lengths following isometric (Gauthier et al.,
50
1993; Cutlip et al., 2004) and eccentric exercise (Cutlip et
al., 2004), implicating metabolic changes as the common
40
ECC factor in the altered shape of the ascending limb of the
ISO
30 FLR following exercise. Here, we showed that isometric
exercise produced the greatest reduction in joint torque
20 at short muscle lengths. Similarly, the greatest reduction
in joint torque following eccentric exercise
10 (55.073.0%), also occurred at the smallest joint angle
tested (551, Fig. 3), corresponding to the shortest muscle
0 length.
50 60 70 80 90 100 110 120 130 140 150 160
Tibiotarsal Joint Angle [degrees] In this study, the eccentric exercise was performed on
the ascending limb and plateau region of the FLR. It has
Fig. 3. Percent decrease in joint torque production immediately been shown that markers of muscle injury, including the
following 50 eccentric contractions (B) and 50 isometric contractions
(’). Visual inspection of the graph shows similar shaped traces for
shift in FLR, are greater on the descending, compared
both the eccentric (ECC) and the isometric (ISO) groups, as the to ascending, limb of the FLR (Whitehead et al., 2003;
greatest loss of torque production following both protocols occurred at Cutlip et al., 2004; Talbot and Morgan, 1998). There-
short muscle lengths. Analysis of the data indicate a significantly fore, it is possible that the contribution of fatigue to the
greater reduction in joint torque in the ECC group compared to the FLR shift following eccentric exercise at long muscle
ISO group at joint angles of 55–701, as indicated by (*). Significance of
po0.05 was reported. Values are means7SE (ECC n=4; ISO n=6).
lengths would be diminished, due to a greater rightward
shift following eccentric exercise.
Since fatigue has been shown to have a greater effect
The contribution of fatigue to the rightward shift of at short compared to long muscle lengths (Gauthier et
the FLR may be associated with the change in shape of al., 1993; Cutlip et al., 2004), torque production is
the FLR following both types of exercise, as the shapes reduced to a greater extent at short compared to long
of the torque–angle curves were similar between the lengths, producing a post-exercise torque–angle rela-
exercise groups (Figs. 1 and 2). Simply, the torque–angle tionship that is altered in shape. Torque decrement at
relationship appears to be rotated counterclockwise short muscle lengths following eccentric exercise is
 ARTICLE IN PRESS
T.A. Butterfield, W. Herzog / Journal of Biomechanics 38 (2005) 1932–1937
similar to that seen following isometric exercise (Fig. 3),
but increased in magnitude for the eccentric compared
to the isometric protocol. Thus, we concluded that
metabolic changes are implicated in the altered shape of
the ascending limb of the FLR following eccentric
exercise. This, in conjunction with the use of curve
fitting to predict the peak of the FLR, although well
accepted (Wood et al., 1993; Jones et al., 1997; Talbot
and Morgan, 1998; Whitehead et al., 1998), may
produce the rightward shift due to fatigue.
5. Conclusion
We demonstrated that a rightward shift in the FLR
following exercise may be partially attributed to the
effects of fatigue. Although it is well accepted that
contractile element damage plays an important role in
the altered mechanical properties of muscle following
eccentric contractions, the role of fatigue with respect to
the shift in peak force production seems to have been
overlooked. Based on the current results, fatigue may be
responsible for up to 50% of the measured rightward
shift in peak torque production following eccentric
exercise. Therefore, the shift in peak torque is not
necessarily a simple and reliable indicator of muscle
damage.
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